Atractylodes lancea volatiles induce physiological responses in neighboring peanut plant during intercropping

Abstract

Aims

Plant volatiles serve as airborne semiochemicals, bridging the interactions between the plant and environment. Intercropping of a Chinese medicinal herb, Atractylodes lancea, with peanut plants greatly improves peanut growth, leading to a reduction of soil-borne disease. The underlying mechanism of peanut responding to the intercropped A. lancea is unknown. We here explored the response of the above- and belowground peanut parts to volatiles produced by the aboveground parts of A. lancea.

Methods

Closed cultivation system was used. Composition of volatiles released by A. lancea plant was first determined using headspace solid phase microextraction–gas chromatography/mass spectrometry (SPME-GC-MS). Then, physiological responses of peanut were explored via enzymes activity assay and root secretions. Changes in the peanut rhizosphere fungal and bacterial communities were analyzed by Illumina sequencing.

Results

The intercropped A. lancea volatiles induced a physiological response in peanut, which includes the increased catalase and phenylalanine ammonia lyase activity in peanut leaf, and improvement of peanut growth. Secretion of organic acids by the peanut root was increased in response to volatile treatment. Pyrosequencing of the whole internal transcribed spacer and 16S rRNA amplicons revealed significant differences in microbial diversity and composition in peanut rhizosphere upon volatile treatment.

Conclusions

In the intercropping, A. lancea volatiles play a key role in influencing the growth of a neighbouring peanut plant, e.g., increasing biomass and affecting root colonization by soil microorganisms, which may increase plant protection against pathogens. Intercropping patterns could be designed accordingly to increase crop performance.

Introduction

Intensive field systems that employ single crop cultivars enhance the degradation of soil quality and environmental carrying capacity, and outbreaks of crop diseases in the agroecosystem, threatening the sustainability of field crops (Brooker et al. 2016). Chemical products, including pesticides, disinfectants, and chemical fertilizers, are widely used to maintain the production of intensive systems (Horrigan et al. 2002; Tao et al. 2005; Carvalho 2017). However, environmental pollution and high input of these chemical products are incompatible with sustainable agriculture (Le Cointe et al. 2016). Therefore, other effective agricultural control strategies, such as elongated rotation of different crop cultivars and optimized cropping patterns, have important potential for improving agricultural production (Boudreau et al. 2015; Brooker et al. 2015).

We have previously examined the possibility of intercropping with traditional medicinal plants for intensive peanut production. Of these, intercropping with Atractylodes lancea was identified as the most effective approach of reducing peanut disease and crop failure (Dai et al. 2009, 2013). However, many important plant–plant, and other, interactions that occur during intercropping with A. lancea remain unknown (Li et al. 2014a, b).

Several mechanisms explaining the effects of intercropping have been proposed (Theunissen and Schelling 1996; Latati et al. 2014; Li et al. 2018). In the intercropping system, underground interactions of plants, e.g., via rhizodeposits, are thought to play a role in nutrient uptake, soil microbial community responses, and, especially, inhibition of targeted pathogens by roots of the adjacent plant. For instance, we demonstrated that A. lancea volatiles and root exudates released into the soil suppress the peanut root rot (Li et al. 2018). Nevertheless, some evidence exists that plants can detect neighboring plant without direct physical contact, which constitutes an important mechanism of plant–plant communication (Heil and Bueno 2007; Loreto et al. 2014). Volatile organic compounds (VOCs) released by a plant can serve as ideal signaling molecules (semio- or info-chemicals), mediating plant interactions over a certain distance (Pinto-Zevallos et al. 2013). A. lancea, a traditional Chinese herb, produces many active volatile compounds that effectively regulate the physiology of an organism (Masuda et al. 2015; Li et al. 2018). A. lancea plant releases VOCs that can trigger specific defensive responses in the neighboring plants (Baldwin et al. 2006; McCormick et al. 2012). It therefore remains to be seen whether neighboring peanut could benefit from an A. lancea VOC-mediated communication.

Plants have developed complex antioxidant defense systems that respond to environmental stimulation. The mitigation of reactive oxygen species (ROS) depended largely upon several antioxidant enzymes such as superoxide dismutase (SOD; EC 1.15.1.1), peroxidase (POD; EC 1.11.1.7), and catalase (CAT; EC 1.11.1.6) (Bowler et al. 1992; Mishra et al. 2008). Plants also contain non-enzymatic ROS-scavengers, generally as a consequence of various (a)biotic stimulations, increased phenylalanine ammonia-lyase (PAL; EC 4.3.1.5) activity was observed, which have been considered part of a defense mechanism. Furthermore, these physiological metabolisms induced by the changing plant growth environments will result in the changes in plant root secretions, which play a central role in plant defense (Baetz and Martinoia 2014). Therefore, exposing upon a plant VOCs, various responses of another neighboring plant, such as the expression of direct physiologic defenses and the secretion of plant metabolites could be induced. This communication process among plants especially under the intercropping system would increase plant resistance when responding environmental stresses.

The rhizosphere is a hot spot of microbial interactions, since exudates released by the plant root are the main food source for microorganisms, and a driver of microbial community structure and composition (Berendsen et al. 2012). Growing evidence suggests that the rhizosphere microbial community determines plant health and productivity by suppressing pathogenic microbes (Mendes et al. 2011), triggering systemic tolerance (Selvakumar et al. 2012), and enhancing plant’s innate immunity (Zamioudis and Pieterse 2012). Therefore, shaping the microbial community composition in the rhizosphere in relation to the plant physiological status is critical for the management of plant growth. However, only few reports have been published on the effect of plant VOCs on the rhizosphere microbial community of a neighboring plant (Hu et al. 2018). This knowledge could potentially empower the adaptation of intercropping system.

In the current study, we hypothesized that VOCs emitted by A. lancea plant can act as signals for the neighboring plant, specifically, elicit physiological responses of peanut in an intercropping system (Fig. 1). To test this, we first determined the composition of VOCs released by A. lancea plant using headspace solid phase microextraction–gas chromatography/mass spectrometry (SPME-GC-MS). We then analyzed the enzymes induced in peanut leaf and the peanut root metabolism changes in response to A. lancea VOCs. Finally, we used Illumina sequencing to determine the rhizosphere fungal and bacterial communities of peanut that respond to A. lancea VOCs.

Fig. 1
figure1

Schematic diagram of A. lancea volatiles mediating peanut responses, from aboveground physiology to plant rhizosphere

Materials and methods

The soil and plants

The soil for pot experiments was collected from an agricultural field in a peanut-planting area (28°13′N, 116°55′E, Yujiang county, China). The sampled field has been planted with peanut for preceding 5 years. A severe incidence of root rot (61.4%) caused by Fusarium oxysporum and F. solani among peanut plants in the last season before sampling was reported, resulting in a relatively low yield (2146 kg ha− 1) (Li et al. 2018). In March 2016, approximately 200 kg soil was randomly collected from the surface layer (0–20 cm) and homogenized for pot cultivation in the greenhouse. The soil was classified as Udic Ferrosol [FAO (1998) classification]. The overall physicochemical properties of the soil were as follows: pH, 4.64; organic matter content, 10.59 g kg− 1; total N, 0.75 g kg− 1; total P, 0.46 g kg− 1; total K, 10.3 g kg− 1; available N, 42.88 mg kg− 1; available P, 13.56 mg kg− 1; and available K, 189.2 mg kg− 1.

The peanut cultivar Guanhua-5 was used for pot cultivation. Guanhua-5 is the main planted variety in the analyzed planting region, and was derived from the parental peanut cultivar Yueyou551-11 by radiation. A. lancea (Thunb.) DC belongs to the family Asteraceae and is a herb used in traditional Chinese medicine.

Experimental design and sample collection

To investigate the physiological response of peanut to the volatiles released by A. lancea, a glass container (length⋅width⋅height = 60 cm⋅20 cm⋅50 cm) was used to contain and cover two pots (Fig S1). First, fresh soil samples (2 kg) were weighed into a pot (length⋅width⋅height = 13 cm⋅8 cm⋅11 cm), and two pots were placed 40 cm apart in a glass container. Peanut seeds were surface-disinfected with 0.5% sodium hypochlorite (NaOCl) for 5 min, and then washed three times in sterile, distilled water. A. lancea was first cultivated in its rhizome for 2 months, and then transplanted to the pots. For the VOC treatment, peanut seed was sown in one pot, and A. lancea seedling with (20-cm high) was placed in another pot. As a control, peanut was planted in both pots in each container. The container experiment was conducted in a greenhouse (day: 30 ± 2 °C, night: 20 ± 2 °C, 60–70% relative humidity). Each treatment included six containers, as replicates. The plants were watered based on the soil moisture.

After 40-d cultivation (the flowering stage), peanut plants were carefully removed from the pots. Three out of six containers were randomly selected per treatment. The soil attached to the roots (the rhizosphere soil) was collected by gentle shaking of plants, and stored at − 20 °C for subsequent analysis of bacterial and fungal community composition. After sampling, the peanut plants were separated into stem leaf and root to determine the growth status. The fresh top leaves of peanut were subsequently stored at − 60 °C for antioxidant enzyme extraction. Peanut plant exudates were collected from the remaining three containers from each volatile treatment and control.

Response of peanut growth and physiological enzymes to A. lancea volatiles

The height and weight of plants, and root fresh weight were determined after rinsing with water, which was then removed using sterilized filter paper. To assess the enzymatic activity, peanut leaves (0.5 g) were first homogenized in potassium phosphate buffer (0.1 mL L− 1, pH 7.4). The homogenate was centrifuged at 2000⋅ g for 10 min at 4 °C, and the supernatant was collected. CAT, SOD, and MDA activities were measured in the supernatant using commercial kits (Jiancheng, Nanjing, China), according to the manufacturer’s instructions. For the PAL assay, leaves (0.5 g) were placed in a pre-chilled mortar with 4.5 mL of extraction buffer (0.05 mL L− 1 boric acid buffer, 5 mM mercaptoethanol, and 0.1 g polyvinylpyrrolidone) and processed. The homogenate was centrifuged at 11,000⋅ g for 15 min at 4 °C. PAL activity was determined in the collected supernatant at 290 nm using a spectrophotometer.

Effect of A. lancea volatiles on peanut root secretions

Peanut roots were first washed with deionized water to remove the adhering soil. The entire root systems of one peanut per container was submerged in a solution of 0.05 mM CaCl2 in a glass beaker (100 mL) wrapped in aluminum foil to prevent light exposure. The beaker was then placed in a biochemical incubator at 14 h-light (30 °C)/10-h dark (25 °C) cycle, and 70–80% humidity. After 24 h, the collected root exudates were filtered through a double layer of Whatman no. 1 filter paper, and freeze-dried at − 60 °C. The lyophilized root exudate powder was dissolved in 0.5 mL of derivatization reagent (BSTFA:TMCS = 99:1) at − 80 °C for 2 h to obtain concentrated root exudate.

The components of peanut root exudates were determined using a GC/MS-CP3800 equipped with a CP-8 column (30 m⋅0.25 mm⋅0.25 µm, Agilent, CA, USA). The conditions used were as follows: shunt ratio, 1:10; ion trap temperature, 200 °C; initial column temperature: 80 °C for 3 min, followed by a ramp up of 5 °C min− 1 to 260 °C for 2 min; carrier gas, helium; column flow rate; 1 mL min− 1. The mass spectra were obtained using the scan mode (total ion count, 35–600 m/z). Compound identity was confirmed by comparing the obtained spectra with the spectral library of the National Institute of Standards and Technology (NIST08). Peak areas of the confirmed components were calculated by using Xcalibur 2.0, and relative amounts of the compounds were calculated on the basis of peak area ratios.

Effect of A. lancea volatiles on microbial community of peanut rhizosphere

Total microbial community DNA was first extracted from approximately 0.5 g of the rhizosphere soil using the FastDNA® SPIN Kit for the soil (MP Biomedicals, Santa Ana, CA, USA) according to the manufacturer’s protocol. Amplicon libraries were prepared using tagged bacterial and fungal universal primers (F515/R806 for bacteria; ITS1F/2043R for fungi), targeting the V4 region of the 16S rRNA gene and the internal transcribed spacers 1, respectively (Caporaso et al. 2011; Zhao et al. 2016). All polymerase chain reactions (PCR) were performed in triplicate in 20-µL mixtures containing 4 µL of 5⋅FastPfu buffer, 2 µL of 2.5 mM dNTPs, 0.8 µL of each primer (5 µM), 0.4 µL of FastPfu polymerase, and 10 ng template DNA. PCR products were resolved on and then extracted from a 2% agarose gel, and further purified using the AxyPrep DNA gel extraction kit (Axygen Biosciences, Union City, CA, USA) and quantified using QuantiFluor™-ST (Promega, Madison, WI, USA) according to the manufacturers’ instructions. Pooled 16S rRNA and internal transcribed spacer (ITS) 1 amplicon samples were sequenced using the MiSeq platform at Majorbio Bio-Pharm Technology Co. Ltd. (Shanghai, China).

Illumina paired-end sequences were processed using the QIIME package (v1.6.0) (Caporaso et al. 2011). Low-quality sequences (< 150 bp in length with an average quality score of < 25) were removed. The reads were trimmed and assigned based on unique 7-base barcodes. The barcode and primer sequences were then removed. The forward and reverse reads were incorporated into full-length sequences based on the thresholds: overlap length > 10 bp and mismatch ratio < 0.2. After screening, filtering, and preclustering, chimeras were detected with USEARCH (Edgar 2013). All operational taxonomic units (OTUs) were identified using UPARSE (v7.1, http://drive5.com/uparse/) with the “greedy” algorithm at a 97% sequence similarity level. The taxonomy of each 16S rRNA gene sequence was analyzed by using the RDP Classifier algorithm (http://rdp.cme.msu.edu/) against the Silva (SSU123) 16S rRNA database (Quast et al. 2013), and ITS sequences against the UNITE database release 7.0 (Kõljalg et al. 2013).

Headspace collection and analysis of A. lancea volatiles

The volatiles released aboveground by A. lancea that has been growing for 40 d (the vegetative stage) were analyzed using SPME-GC-MS. A pot planted with A. lancea was covered with a plexiglass hood for volatile acquisition. The SPME head was inserted at the top of the plexiglass hood and the fibers (75 µm carboxen/polydimethylsiloxane, Supelco, Bellefonte, PA, USA) were exposed to the hood headspace at room temperature for volatile collection (Fig S2). After 60 min, the fiber heads were withdrawn, and the SPME heads were stored at − 20 °C until GC-MS analysis. The same protocol for volatile collection was followed for three A. lancea plants. The empty pots without A. lancea plantwere also sampled as the control, to define volatile background levels. Samples were analyzed using a GC-MS (6890N-5975) equipped with a HP-5MS column (30 m⋅0.25 mm inner diameter⋅ 0.25 µm film thickness). Trapped compounds were desorbed using an automated thermal desorber (TD-100, Markes International Ltd., Llantrisant, UK) at 250 °C for 10 min, cryofocused at − 10 °C, and then transferred to an HP-5 capillary column (30 m⋅0.25 mm inner diameter⋅0.25 µm film thickness). Helium was used as a carrier gas. The oven temperature was held at 60 °C for 1 min, and then ramped up at 10 °C min− 1 to 300 °C under a column flow of 1.2 mL min− 1. Mass spectra were obtained using the scan mode (total ion count, 35–600 m/z). The electron impact energy was 70 eV and the filament current was 50 µA. The putative identities of the compounds were assigned by comparison with mass spectra from the NIST database, with minimum match factor 70. The library mass spectra of the compounds were then pooled into a sub-library, and analyzed by further automated data evaluation by automated mass spectral deconvolution and identification system (AMDIC) software (v2.64) (Stein 1999).

Statistical analysis

Data were analyzed using SPSS software (IBM SPSS Statistics version 24.0, Armonk, NY, United States), considering the mean of three biological replicates with standard deviation (SD) for plant growth and enzyme activity. Tukey’s HSD test of analysis of variance (ANOVA) was used to compare the differences in plant growth and physiological indices between treatments (p < 0.05). To compare the composition and structure of the bacterial and fungal communities in peanut rhizosphere, principal coordinate analyses (PCoA) was performed using Fast UniFrac analysis, evaluating the degree of similarity between the volatile and control treatments. Differences of the relative abundance of the fungal (≥ 0.5%) and bacterial (≥ 1%) phylotypes in peanut rhizosphere between volatile and control treatments were compared using STAMP (v8.30) with the gplots package.

Results

Effects of A. lancea volatiles on peanut growth and physiological enzymes

We first determined the composition of VOCs emitted by the aboveground parts of A. lancea using SPME-GC-MS. The volatile spectrum contained 19 compound peaks. Seven compounds were identified by comparing their mass spectra with those deposited in the NIST database (Fig S3), including three terpenes, one alkane, one aromatic hydrocarbon, and one ester (Table 1).

Table 1 Volatile organic compounds produced by A. lancea leaves detected using SPME-GC-MS analysis. Only compounds identified based on the retention indices and mass spectra are shown

In the experimental system used in the current study, peanut and A. lancea did not interact underground because they were grown in independent pots. Nevertheless, the aboveground parts of peanut were exposed to volatiles released by A. lancea leaves. Peanuts planted in monocropped soils showed overall growth improvement upon exposure to A. lancea volatiles (Fig. 2a, b), with a significant response of peanut plant weight to the volatiles. CAT and PAL activities in peanut leaves exposed to A. lancea volatiles were 30.5% and 71.9% higher, respectively (p < 0.05), than those in the control plants, but with no difference in SOD activity (Fig. 2c, d, e). Accordingly, A. lancea volatiles significantly reduced the accumulation of MDA in peanuts planted in monocropped soil (Fig. 2f). We did not observe Fusarium root rot, prevalent in peanut monoculture, in the experimental pots, with or without A. lancea treatment.

Fig. 2
figure2

Effect of A. lancea volatiles on plant growth and physiological indices of peanut planted in monocropped soil. Control, peanut pots without A. lancea; Volatile, peanut and A. lancea plants, which emit volatiles during growth. CAT, catalase; PAL, phenylalanine ammonia-lyase; SOD, superoxide dismutase; MDA, malondialdehyde. The means and standard deviation from three biological replicates are shown. Different letters above the bars indicate statistically significant differences (p < 0.05) between the control and volatile treatments, according to Tukey’s HSD test

A. lancea volatiles induce changes in peanut root secretions

We next identified 15 compounds in peanut root exudates (organic acids, ether, phenolic acid, alcohol, alkanes, arene, alkene, hydroxy amine, and saccharide) (Fig S4). Organic acids were the dominant components, accounting for over 35% of the identified compounds. A. lancea volatiles induced the secretion of some compounds while reducing the secretion of others (Table 2).

Table 2 Composition and relative content of peanut root exudates in plants from the control and volatile treatments

A. lancea volatiles affect the rhizosphere microbial community of peanut

We have obtained 188,806 high-quality bacterial 16S rRNA gene sequences and 273,514 fungal ITS1 sequences from the rhizosphere soil samples by high-throughput pyrosequencing. The sequences were clustered into 2,322 bacterial OTUs and 534 fungal OTUs at 97% sequence similarity, accordingly. An investigation of the categorized 18 bacterial phyla revealed that members of Proteobacteria, Chloroflexi, and Actinobacteria were prominent in the peanut rhizosphere, accounting for over 80% of the classified sequences (Table S1). Across the six fungal phyla, Ascomycota and Basidiomycota accounted for over 60% of sequences (Table S2).

Lineage-specific, weighted UniFrac and (PCoA) revealed distinctive differences in both fungal and bacterial community compositions of peanut rhizosphere in treated and control plants (Fig. 3). With respect to the microbial diversity, A. lancea volatiles significantly increased the OTU number and Shannon-Wiener index of the bacterial community. Furthermore, fungal OTU number also significantly increased in the peanut rhizosphere of volatile-exposed plants compared with the control (Table S3).

Fig. 3
figure3

Lineage-specific weighted UniFrac analysis of microbial communities in the peanut rhizosphere. The first (PC1) and second (PC2) principal coordinates explain the variations in OTU composition of the bacterial (a) and fungal community (b) in the rhizosphere of peanut exposed to A. lancea volatiles in comparison with control plants. Control, peanut pots without A. lancea; Volatile, peanut and A. lancea, which emit volatiles during growth

To gain insight into the effects of A. lancea volatiles on the composition of the bacterial community in peanut rhizosphere, we performed one-way ANOVA for different taxonomic groups for the two treatments. A. lancea volatiles significantly increased the relative abundances of Chloroflexi and Cyanobacteria in peanuts planted in monocropped soil, and reduced the relative abundance of Proteobacteria and Bacteroidetes (Table S1). Within Proteobacteria, the relative abundance of Xanthomonadaceae and Alcaligenaceae in the peanut rhizosphere significantly decreased upon A. lancea volatile treatment (Fig. 4a). However, the relative abundance of Pseudonocardiaceae within Actinobacteria, Gemmationadaceae within Gemmatimonadetes, and a no-rank family in Cyanobacteria in the peanut rhizosphere significantly increased (p < 0.05), whereas that of Chitinophagaceae and Sphingomonadaceae within Bacteroidetes, and Microbacteriaceae within Actinobacteria decreased compared with the control (Fig. 4a).

Fig. 4
figure4

Abundance analysis of microbes in the peanut rhizosphere. Mean proportion (n = 03), differences, and p-values of the most abundant bacterial families (16S rDNA sequences > 1%) (a) and fungal genera (ITS sequences > 0.5%) (b) in the rhizosphere of peanut exposed to A. lancea volatiles in comparison with control plants

Across the fungal phylotypes, A. lancea volatile treatment significantly enhanced the relative abundance of Basidiomycota, Zygomycota, and Glomeromycota in the peanut rhizosphere (p < 0.05), while that of Ascomycota decreased in the peanut rhizosphere upon volatile treatment (Table S2). Within the phylum Ascomycota, A. lancea volatile exposure significantly decreased the relative abundance of an unclassified genus in Trichocomaceae and Penicilliumin in the peanut rhizosphere (p < 0.05), whereas the relative abundances of Geminibasidium, Mortierella, and Cryptococcus increased (Fig. 4b).

Discussion

Interactions of the underground parts of diverse plants in the field, and the resultant improvement of soil nutrient content and the reduction in soil pathogen inoculums, are often uncovered in practice (Hauggaard-Nielsen et al. 2009; Duragannavar et al. 2013). However, the belowground interactions of a neighboring plant mediated by aboveground plant volatiles are relatively unknown. In the current study, we found that the volatiles released by the intercropped A. lancea leaves improved plant growth and resistance of the neighboring peanut. This effect was illustrated by the changes in the peanut root exudate composition and in the associated rhizosphere communities. For plant volatiles to play such complex roles, the neighboring plants have to be particularly sensitive to metabolites, released in sufficient quantities so as to affect the neighboring plants (Baldwin 2010). Terpenes were three of abundant A. lancea leaf volatiles identified herein. Indeed, terpenes are released by A. lancea stem, leaf, and rhizome (Guo et al. 2006; Ahmed et al. 2016). Terpenoids especially are responsible for the chemical diversity of plant volatiles, and appear to support plant–plant communication and elicit plant resistance (Tholl et al. 2006; Yuan et al. 2009; de Vos and Jander 2010). These observations suggest plant volatiles affect the underground parts by affecting the aboveground parts and constitute new evidence for the role of chemical-mediated mechanisms in intercropping.

Plant responses to chemical signals affect growth pattern and biomass allocation (Ninkovic 2003). Exposing potato to volatiles from onion plant alters its physiological profile, and this response deters the host-seeking Myzus persicae (Ninkovic et al. 2013). Biotic or abiotic environmental stresses widely activate antioxidant protective systems to remove excess reactive oxygen species (G), maintaining normal physiological and developmental processes in a plant (Bela et al. 2015; Navrot et al. 2007). We showed here that A. lancea volatiles induced the CAT and PAL activities in peanut leaves. Similar induction of antioxidant enzymes in response to volatile compounds has been reported for other species. For instance, trans-2-hexenal increases the expression of relevant enzyme-encoding genes in tomato fruit (Guo et al. 2015). Further, resistance-related genes in maize are rapidly expressed in plants previously exposed to volatiles released by caterpillar-infested plants (Turlings et al. 1998). Therefore, the low doses of volatiles released by A. lancea prime the neighbor peanut for physiological resistance, as a response that is more rapid than phenotypic change (Heil and Karban 2010). Despite these observations, the manner whereby volatiles affect plant antioxidant protective systems on molecular levels remains to be determined.

Accumulating evidence indicates that the metabolic processes of plant play a major role in determining the composition of root exudates (Bertin et al. 2003; Baetz and Martinoia 2014). We therefore hypothesized that the changes in peanut enzymatic activity induced by A. lancea volatiles would influence the peanut root secretions. In the current study, we have compared the profiles of root exudates from peanuts intercropped with A. lancea (volatile treatment)versus the monoculture without A. lancea volatiles. Indeed, A. lancea volatiles induced the secretion of phenolic and organic acids, especially benzoic acid, glyceric acid, nonanoic acid, and myristic acid, by the peanut root. PAL is a starting-point enzyme in the phenolic production pathway prerequisite for organic acid production. For instance, it was reported that increased organic acid content in the root exudates accompanied PAL activation (Fang et al. 2013; Juszczuk et al. 2004). Therefore, the increase of phenolic and organic acids in peanut root exudates could be a result of a peanut enzymatic activity response to the volatiles, such as increased PAL activity. In addition, CAL activation in chickpea induces citrate secretion and efflux of other organic acids, improving plant root Aluminum tolerance (Aggarwal et al. 2015; Sharma et al. 2016). The increased amount of organic acids in root exudates observed in the current study may promote the resistance of peanut rhizosphere to biotic stress, as accumulation of pathogenic fungi is frequently reported in consecutive monocultures of agricultural crops (Lu et al. 2013; Li et al. 2014a, b). Interestingly, root exudates of a resistant peanut cultivar contain more phenolic acids than those of a susceptible cultivar (Li et al. 2013). Collectively, the findings of the current and other studies suggest that the direct role of plant volatiles extends to protection against biotic stress in the soil (Lanoue et al. 2010).

Bacterial and fungal communities in the peanut rhizosphere following the A. lancea intercropping differed greatly from those of the peanut monoculture, despite of planting in the same soil. An increasing body of evidence suggests the important effect of rhizosphere microbial community on plant health (Sanguin et al. 2009; Xiong et al. 2017; Wallenstein 2017). For most plant species, successive monoculture results in a build-up of specialized plant pathogens, and the decrease of rhizosphere microbial diversity (Zhou and Wu 2012). In the current study, A. lancea intercropping significantly enhanced the OTU numbers in bacterial and fungal communities in the peanut rhizosphere compared with the monoculture. This could be attributed to the improvement of peanut physiology and root secretions induced by A. lancea volatiles. Many compounds in the root exudates act as substrates, or chemotactic or signaling molecules to orchestrate changes in the rhizosphere microbial community (Dennis et al. 2010; Chaparro et al. 2014; Hu et al. 2018). Therefore, the findings of the current study suggest that a plant rhizosphere community can be indirectly affected by volatiles released by a neighboring plant.

Among the bacterial taxa identified in the peanut rhizosphere, A. lancea intercropping induced a significant decline in the relative abundance of Xanthomonadaceae, Sphingomonadaceae, and Microbacteriaceae. Several species and subspecies within Microbacteriaceae and Xanthomonadaceae are either plant pathogens or putative plant pathogens (Evtushenko and Takeuchi 2006; MhedbiHajri et al. 2011; Mansfield et al. 2012). Although some antimicrobials, e.g., certain phenolics and organic acids in root exudates were reported to defend plant roots from pathogens colonization (Baetz and Martinoia 2014), whether the increased phenolic acids of peanut root exudates in responding to A. lancea intercropping suppress these taxa colonizing the peanut rhizosphere need investigate in vitro. In addition to the direct suppression of certain antimicrobials in root exudates, the possibility of their reduced prevalence may also be involved in the antagonistic effects of beneficial microbes that were recruited by the induced compounds of peanut root exudates in responding to A. lancea intercropping. For instance, the relative abundance of Pseudonocardiaceae and Gemmationadaceae significantly increased in the peanut rhizosphere of A. lancea intercropping. Pseudonocardiaceae, an actinobacterial family, are frequently isolated and detected in the plant root as endophytes, and are usually considered to be plant growth-promoting soil bacteria (Qin et al. 2009; Lewin et al. 2016; Goel et al. 2017). For fungal composition, peanut rhizosphere in monoculture contained more Ascomycetes than Basidiomycetes, while the latter were dominant in the intercropping treatment group. Since Ascomycetes contains the most plant pathogens (Lu et al. 2003; Wang et al. 2015) and antimicrobial activities of Basidiomycetes strains are frequently reported (Srivastava and Sharma 2011), the change in the Ascomycetes to Basidiomycetes ratio upon A. lancea intercropping compared with peanut monoculture may indicate increased resistance of the peanut rhizosphere to root rot that is often observed in the peanut monocropped soil. Furthermore, the relatively low abundance of Fusarium in the peanut rhizosphere observed in the current study is in agreement with previous reports on the limited Fusarium abundance in the plant rhizosphere (Shen et al. 2015; Li et al. 2018). This may be attributed to the short cultivation period of peanut or Fusarium-unpermissive conditions of the rhizosphere environment.

In converse to the intensive agricultural systems with monocultures, intercropping reveals many potential advantages in enhancing agricultural sustainability. For instance, a recent survey concluded that intercropping reduced disease severity relative to monocrops in 79% of studies involving fungal pathogens, and 100% of bacterial studies (Boudreau 2013). Although understanding the mechanisms by which disease behaves in an intercrop is critical for furthering practical application, the identity of intercrops is a prerequisite factor for their effectivity. The current study adds a new dimension to the intercropping applications, showing that volatiles from A. lancea not only induced physiological resistance of the neighbouring peanut, but microbial community composition was also shed light onto peanut root colonization. Obviously these mechanisms, although less recognized, have been operating during intercropping, we thus argue that intercropping with A. lancea and use of its allelopathic volatiles have a strong potential for improving agricultural production and sustainable control of plant diseases.

Conclusions

We here showed that the aboveground volatiles of the intercropped A. lancea play an important role as plant signals that elicit physiological resistance of adjacent peanut. The effect can be extended to the peanut rhizosphere despite the lack of physical interaction between the plants underground. The subsequent alteration of rhizosphere communities in response to A. lancea intercropping may improve peanut resistance, at least partially explaining the reduction of peanut disease associated with intercropping. This observation is crucial to the understanding of the management of diverse crop types, highlighting the effect on plant performance and consequences of plant communication via airborne signals. Furthermore, plant volatiles have strong practical potential as compounds that boost plant resistance to disease.

Data availability

All data generated or analyzed during this study are included in this published article and its supplementary information files.

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Acknowledgements

We thank Prof. Wietse de Boer at the Netherlands Institute of Ecology (NIOO-KNAW) for help during the preparation of the manuscript, and colleagues from our research group (others than the authors) for assistance in conducting the field experiments. This study was supported by the National Natural Science Foundation of China (41671306, 41371290); the Excellent Youth Foundation of Jiangsu Province (BK20190040); China Agriculture Research System (CARS-13).

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X.L. and X.W. conceived the project and designed the study; Y.Z. conducted the experiments; X.L. and Z.Y. analyzed the data with assistance from X.W. and C.D.; X.L. and Z.Y. contributed to the drafting of the initial manuscript; all co-authors revised, read, and approved the final manuscript.

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Correspondence to Xingxiang Wang.

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Li, X., Yang, Z., Zhang, Y. et al. Atractylodes lancea volatiles induce physiological responses in neighboring peanut plant during intercropping. Plant Soil (2020). https://doi.org/10.1007/s11104-020-04615-z

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Keywords

  • Plant volatile
  • Physiological response
  • Root exudate
  • Rhizosphere microbial community